RESEARCH ARTICLE Population productivity of shovelnose rays: Inferring the potential for recovery 1,2 3 4 Brooke M. D'AlbertoID *, John K. Carlson , SebastiaÂn A. Pardo , Colin 1 A. SimpfendorferID 1 Centre for Sustainable Tropical Fisheries and Aquaculture & College of Science and Engineering, James Cook University, Townsville, Queensland, Australia, 2 CSIRO Oceans and Atmosphere, Hobart, Tasmania, Australia, 3 NOAA/National Marine Fisheries Service±Southeast Fisheries Science Center, Panama City, FL, United States of America, 4 Biology Department, Dalhousie University, Halifax, NS, Canada a1111111111 * [email protected] a1111111111 a1111111111 a1111111111 a1111111111 Abstract There is recent evidence of widespread declines of shovelnose ray populations (Order Rhi- nopristiformes) in heavily fished regions. These declines, which are likely driven by high demand for their fins in Asian markets, raises concern about their risk of over-exploitation OPEN ACCESS and extinction. Using life-history theory and incorporating uncertainty into a modified Euler- Citation: D'Alberto BM, Carlson JK, Pardo SA, Lotka model, the maximum intrinsic rates of population increase (rmax) were estimated for Simpfendorfer CA (2019) Population productivity nine species from four families of Rhinopristiformes, using four different natural mortality of shovelnose rays: Inferring the potential for estimators. Estimates of mean rmax, across the different natural mortality methods, varied recovery. PLoS ONE 14(11): e0225183. https://doi. -1 org/10.1371/journal.pone.0225183 from 0.03 to 0.59 year among the nine species, but generally increased with increasing maximum size. Comparing these estimates to rmax values for other species of chondrichth- Editor: Heather M. Patterson, Australian Bureau of Agricultural and Resource Economics and yans, the species Rhynchobatus australiae, Glaucostegus typus, and Glaucostegus Sciences, AUSTRALIA cemiculus were relatively productive, while most species from Rhinobatidae and Trygonor- Received: April 4, 2019 rhinidae had relatively low rmax values. If the demand for their high-value products can be addressed then population recovery for some species is likely possible, but will vary depend- Accepted: October 30, 2019 ing on the species. Published: November 21, 2019 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Introduction Data Availability Statement: All relevant data are An estimated 25% of chondrichthyan (sharks, rays and chimeras) populations have an elevated within the paper and its Supporting Information risk of extinction [1], raising significant ecological and conservation concerns [2±4]. Chon- files. drichthyans, generally have low biological productivity (slow growth, late maturity, few off- Funding: This project was funded by the Shark spring, and long generational times), which limits their ability to recover from population Conservation Fund (Small Grant Program 2018 to declines [5, 6]. Declines of chondrichthyan populations are typically the result of the rapid BMD), a philanthropic collaborative pooling expansion of fisheries [7±9] and the globalisation of trade [10, 11], and can be exacerbated by expertise and resources to meet the threats facing habitat degredation [12]. Compared to other chondrichthyans, larger elasmobranchs (sharks the world's sharks and rays. The Shark Conservation Fund is a project of Rockefeller and rays, Subclass Elasmobranchii) have some of the lowest intrinsic rates of population Philanthropy Advisors. The corresponding author increase [13, 14], and as a result are unlikely to sustain high levels of fishing pressure before (BMD) is supported through an Australian population collapse [15±18]. PLOS ONE | https://doi.org/10.1371/journal.pone.0225183 November 21, 2019 1 / 24 Population productivity of shovelnose rays Government Research Training Program The order Rhinopristiformes is considered one of the most threatened orders of marine fish Scholarship (RTPS). The scientific results and [1, 19], and comprises five families: sawfish (Pristidae), giant guitarfish (Glaucostegidae), wed- conclusions, as well as any views or opinions gefish (Rhinidae), guitarfish (Rhinobatidae) and banjo rays (Trygonorrhinidae) (Table 1) [19, expressed herein, are those of the author(s) and do not necessarily reflect those of NOAA or the 20]. These large rays are strongly associated with soft-bottom habitats in shallow (<100 m) Department of Commerce. The funders had no role tropical and temperate coastal waters [21±23], resulting in high exposure to intensive and in study design, data collection and analysis, expanding fisheries [24]. These coastal habitats are under threat from anthropogenic influences, decision to publish, or preparation of the which is also a significant threat for these rays [25, 26]. They are very susceptible to overexploi- manuscript. tation as a result of their large body size [1], high catchability by multiple gear types [27], and Competing interests: The authors have declared use of inshore habitat in some of the world's most heavily fished coastal regions [28±30]. that no competing interests exist. There is increasing evidence of historical and contemporary declines in landings and catch rates for wedgefishes, giant guitarfishes, guitarfishes and banjo rays (herein collectively referred to as shovelnose rays), of up to 80% throughout most of their ranges [24], including Indonesia [31], South Africa [32], Madagascar [33], Mozambique [34], Tanzania [35], Arabian Seas and surrounding region [19, 36], India [37] and Brazil [38]. Many species of shovelnose rays are facing a high to extremely high risk of extinction in the wild [24, 39, 40]. While there are very few directed fisheries (e.g. Indonesian tangle-net fishery [27]) for shovelnose rays, they are typically retained in commercial and artisanal fisheries as by-products for their highly valued fins and good quality meat [24, 41, 42]. Wedgefish and giant guitarfish fins are consid- ered the highest grade fins [7, 25, 31, 43]. The reported declines of landings and catches of shovelnose rays are likely to be primarily driven by the international shark fin trade as they are prevalent in fin trading hubs such as Hong Kong [44] and Singapore [45, 46]. There is consid- erable concern that shovelnose rays, in particular wedgefishes and giant guitarfishes, are fol- lowing a similar pattern of global decline as the sawfishes [19, 24]. All five species of sawfish declined rapidly over 30 years throughout their range, driven by unregulated fisheries, the interational fin trade, and delayed scientific attention [47±50]. Yet despite a global conserva- tion strategy [25], restriction of international trade (i.e. listing on Convention on International Trade in Endangered Species of Wild Fauna and Flora [CITES] Appendix I), and evidence that some species of sawfish have the ability to recover from fishing pressure [51], the recovery of the populations is projected to take at least several decades. Precautionary management and conservation of shovelnose rays is therefore vital to maintain their populations. Currently, fisheries for shovelnose rays are not regulated through national or regional spe- cies-specific fishing regulations. The magnitude of declines in landings in heavily fished regions, and the subsequent conservation issues have attracted the focus of major international management conventions and agencies, such as the Convention on the Conservation of Migratory Species of Wild Animals (CMS; Rhynchobatus australiae and Rhinobatos rhinobatos listed on the Appendix II) [52], the non-binding CMS Memorandum of Understanding on the Conservation of Migratory Sharks (CMS Sharks MOU; R. australiae, Rhynchobatus djiddensis, Rhynchobatus laevis, and R. rhinobatos listed on Annex 1) [53], and CITES (families Rhinidae and Glaucostegidae listed on Appendix II) [54]. For CITES Appendix II listed species, the international trade of wild specimens must be legal and sustainable, which is dependent on provisions such as the export is not detrimental to wild populations (through a positive non- detriment finding, NDF), the specimens are legally sourced, and shipments are accompanied by export, import or re-export permits [55]. While the CMS Appendix II listing acts as a framework for the Range States (any Party [nation] that exercises jurisdiction over any part of the range of that migratory species) of the migratory species that have unfavourable conserva- tion status, and requires international agreements [56]. These international agreements pro- vide a global platform and legal foundation for the conservation and sustainable use of internationally traded species (CITES), and migratory species and their habitat (CMS) [55]. Given the global concerns for this group of species and the importance of trade in their high- PLOS ONE | https://doi.org/10.1371/journal.pone.0225183 November 21, 2019 2 / 24 Population productivity of shovelnose rays Table 1. The nine species of shovelnose rays in this study. Listed is their threat status according the International Union of Conservation of Nature's (IUCN) Red List of Threatened Species, and whether the species are listed on the appendixes of CITES, and/or CMS, and the CMS Sharks MOU (MOU). IUCN categories are CR, Critically Endangered; EN, Endangered; VU, Vulnerable;